Molecular Regulation of Flowering Time in Grasses

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Molecular Regulation of Flowering Time in Grasses agronomy Review Molecular Regulation of Flowering Time in Grasses Fiorella D. B. Nuñez 1 and Toshihiko Yamada 2,* 1 Graduate School of Environmental Science, Hokkaido University, Kita 10 Nishi 5, Sapporo, Hokkaido 060-0810, Japan; fi[email protected] 2 Field Science Center for Northern Biosphere, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan * Correspondence: [email protected]; Tel.: +81-11-706-3644 Academic Editors: John W. Forster and Kevin F. Smith Received: 29 November 2016; Accepted: 13 February 2017; Published: 20 February 2017 Abstract: Flowering time is a key target trait for extending the vegetative phase to increase biomass in bioenergy crops such as perennial C4 grasses. Molecular genetic studies allow the identification of genes involved in the control of flowering in different species. Some regulatory factors of the Arabidopsis pathway are conserved in other plant species such as grasses. However, differences in the function of particular genes confer specific responses to flowering. One of the major pathways is photoperiod regulation, based on the interaction of the circadian clock and environmental light signals. Depending on their requirements for day-length plants can be classified as long-day (LD), short-day (SD), and day-neutral. The CONSTANS (CO) and Heading Date 1 (Hd1), orthologos genes, are central regulators in the flowering of Arabidopsis and rice, LD and SD plants, respectively. Additionally, Early heading date 1 (Ehd1) induces the expression of Heading date 3a (Hd3a), conferring SD promotion and controls Rice Flowering Locus T 1 (RFT1) in LD conditions, independently of Hd1. Nevertheless, the mechanisms promoting flowering in perennial bioenergy crops are poorly understood. Recent progress on the regulatory network of important gramineous crops and components involved in flowering control will be discussed. Keywords: flowering; Arabidopsis; grasses; photoperiod; circadian clock 1. Introduction Global climate change and energy security issues have promoted interest in the production and increased availability of alternative energy sources. Lignocellulosic biomass is a promising feedstock source for biorefineries producing biofuel, which can mitigate greenhouse gas emissions [1–3] and reduce dependency on fossil oil [4,5]. Perennial C4 bioenergy crops such as switchgrass (Panicum virgatum L.) and Miscanthus spp. provide good targets as non-edible plant species [6–8] having advantages with regard to land utilization and the avoidance of conflict with food security [9–11] to provide efficient production systems at low cost. One of the most important traits in the plant life cycle is the timing of flowering, the floral transition between the vegetative and reproductive phases of plant development [12,13]. Consideration of flowering time is an important strategy in the cultivation of grain crops in northern latitudes. Early flowering is useful in regions where growing seasons are short to enhance grain yield stability by avoiding drought or adverse temperatures [14–16]. Flowering time is also a major determinant of biomass yield in perennial C4 bioenergy crops, because delayed flowering time allows an extended period of vegetative growth and produces more biomass. Thus, earlier flowering will produce lower yields than late flowering in terms of feedstock production [17]. However, biomass potential also depends on environmental conditions. In switchgrass, lowland ecotypes that originate from southern areas flower later in high latitude areas, but the yield advantages of these southern switchgrasses are often not realized at northern latitudes due to high winter mortality [18]. Agronomy 2017, 7, 17; doi:10.3390/agronomy7010017 www.mdpi.com/journal/agronomy Agronomy 2017, 7, 17 2 of 10 Natural variation in flowering time is related to latitude in several plant species. Migration of plants into different latitudes often require the adoption of different signals to induce flowering and promote adaptive responses to diverse growing seasons [19]. Factors such as photoperiod and temperature that vary over large geographical scales are involved [20]. Plants possess an internal biological clock providing circadian rhythms that respond to fluctuations in day-length and thus anticipate upcoming seasonal changes [21] to regulate flowering. Depending on their requirements for day-length (light period in a 24-h cycle) to promote flowering, plants can be classified as long-day (LD) plants when photoperiod exceeds a critical day-length, short-day (SD) plants when photoperiod is shorter than a critical day-length and day-neutral plants when flowering occurs irrespective of day-length [22–24]. Winter annuals (e.g., wheat (Triticum aestivum L.)), biennials (e.g., sugar beet (Beta vulgaris L.)) and numerous perennials (e.g., orchardgrass (Dactylis glomerata L.)) are obligatory LD plants. These plants, however, flower only after vernalization during a cold period [23]. The molecular basis of flowering time regulation has been extensively studied using classical Quantitative Trait Loci (QTL) approaches in model plant species such as Arabidopsis thaliana [25–27], a LD plant, and rice (Oryza sativa L.), a SD plant [28]. Grasses have multiple pathways to control flowering time but only some of them are conserved in Arabidopsis thaliana (L.) Heynh. [29]. These studies have been crucial in establishing the multiple pathways that control flowering, of which the photoperiod pathway is of major importance [30]. The use of model species has played a major role in understanding the molecular mechanisms involved in flowering time to help in the genetic improvement of crop development. Nevertheless, little is known about the mechanisms promoting flowering in perennial C4 bioenergy crops. In this review, we discuss recent progress concerning the regulatory network and components involved with flowering control in different species including C4 grasses such as sorghum (Sorghum bicolor (L.) Moench), switchgrass and Miscanthus spp. To understand how plants initiate flowering is a crucial step in developing selection criteria in breeding programs of grasses used as bioenergy crops. 2. Conservation and Divergence in Flowering Pathways 2.1. Arabidopsis and Rice In the last decades, studies on the model plant Arabidopsis have revealed that molecular mechanisms discovered in that species are evolutionally conserved in other species [15]. Genetic approaches in Arabidopsis have identified three genes that control flowering: GIGANTEA (GI)—CONSTANS (CO)—FLOWERING LOCUS (FT) [15,28]. Loss of function mutations in each gene for flowering control delay flowering under LD conditions but no effect is produced under SD [31]. GI is a key regulator of the photoperiodic pathway and in the evening promotes CO transcription under LD conditions [32]. The most extensively gene studied in Arabidopsis flowering is CO that confers LD responses. CO encodes a B-box zinc finger transcription factor and CCT domain genes that promote flowering under LD conditions and activate the expression of FT [33–35], a major component of the florigen that induces flower differentiation [29]. Its inactivation causes flowering delay, while its over-expression induces early flowering. CO and FT are expressed in the phloem and act there to promote flowering [31]. This signalling pathway is conserved in rice: OsGI-Hd1-Hd3a [28], mediated by LD responses. OsGIGANTEA (OsGI) acts an activator of Heading date1 (Hd1), an ortholog of CO, and controls flowering time by modulating rhythmic flowering under SD [36]. Hd1 encodes a zinc finger type transcriptional activator with the conserved CCT (CO, CO-like, TIMING OF CAB EXPRESSION1 (TOC1)) domain [15,37]. In contrast to Arabidopsis CO, Hd1 promotes Heading date 3a (Hd3a) expression in SD but expression is modified in LD conditions [38,39] where Hd1 function is converted into a repressor. Rice involves at least two flowering pathways that control the expression of the florigens: Hd1 that is conserved in rice and Arabidopsis, and Early heading date 1(Ehd1), without an ortholog in Arabidopsis [39,40] (Figure1). Moreover, Grain Number, Plant Height, and Heading Date7 (Ghd7) is unique in grasses [16]. Ehd1 is a B-type response regulator that induces the expression of Hd3a in rice, Agronomy 2017, 7, 17 3 of 10 conferringAgronomy SD2017, promotion 7, 17 of flowering in the absence of a functional allele of Hd1. It also controls3 of 10 Rice Flowering Locus T (RFT) Hd1 Hd1 independently of Hd1 [40].gene In inLD LD conditions conditions Hd1 independently acts as a flowering of repressor[40]. In LD inhibiting conditions Hd3a actsexpression as a flowering but promotes repressor its inhibiting expressionHd3a and expressionsubsequent butflowering promotes in SD its [41]. expression Ghd7 is a and small subsequent protein floweringwith a CCT in SD‐domain[41]. Ghd7that repressesis a small Ehd1 protein expression with aand CCT-domain downstream that Hd3a/RFT1 represses expressionEhd1 expression in LD andconditions downstream to delayHd3a/RFT1 floweringexpression [42–45]. in Recent LD conditions studies demonstrated to delay flowering that the [42 interaction–45]. Recent between studies demonstratedGhd7 and Hd1 that can the play interaction a critical between role in repressingGhd7 and Hd1Ehd1can. Under play SD a critical conditions role Hd1 in repressing activates theEhd1 . Underexpression SD conditions of Ehd1Hd1 at nightactivates but thenot expressionin the day ofwhileEhd1 underat night LD but conditions not in the Hd1 day represses while under its LDexpression conditions inHd1 the repressesmorning.
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